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557
Covariance in species diversity and facilitation among
non-interactive parasite taxa : all against the host
B. R. KRASNOV 1*, D. MOUILLOT 2, I. S. KHOKHLOVA 3, G. I. SHENBROT 1
and R. POULIN 4
1
Ramon Science Center and Mitrani Department of Desert Ecology, Jacob Blaustein Institutes for Desert Research,
Ben-Gurion University of the Negev, P.O. Box 194, Mizpe Ramon 80600, Israel
2
UMR CNRS-UMII 5119 Ecosystemes Lagunaires, University of Montpellier II, CC093, FR-34095 Montpellier Cedex 5,
France
3
Desert Animal Adaptations and Husbandry, Wyler Department of Dryland Agriculture, Jacob Blaustein
Institutes for Desert Research, Ben-Gurion University of the Negev, Beer Sheva 84105, Israel
4
Department of Zoology, University of Otago, P.O. Box 56, Dunedin, New Zealand
(Received 25 February 2005; revised 16 March 2005; accepted 16 March 2005)
SUMMARY
Diﬀerent parasite taxa exploit diﬀerent host resources and are often unlikely to interact directly. It is unclear, however,
whether the diversity of any given parasite taxon is indirectly inﬂuenced by that of other parasite taxa on the same host.
Some components of host immune defences may operate simultaneously against all kinds of parasites, whereas investment
by the host in speciﬁc defences against one type of parasite may come at the expense of defence against other parasites. We
investigated the relationships between the species diversity of 4 higher taxa of ectoparasites (ﬂeas, sucking lice, mesostigmatid mites, and ixodid ticks), and between the species richness of ectoparasites and endoparasitic helminths, across
diﬀerent species of rodent hosts. Our analyses used 2 measures of species diversity, species richness and taxonomic
distinctness, and controlled for the potentially confounding eﬀects of sampling eﬀort and phylogenetic relationships among
host species. We found positive pairwise correlations between the species richness of ﬂeas, mites and ticks ; however, there
was no association between species richness of any of these 3 groups and that of lice. We also found a strong positive
relationship between the taxonomic distinctness of ecto- and endoparasite assemblages across host species. These results
suggest the existence of a process of apparent facilitation among unrelated taxa in the organization of parasite communities.
We propose explanations based on host immune responses, involving acquired cross-resistance to infection and interspeciﬁc variation in immunocompetence among hosts, to account for these patterns.
Key words: ectoparasites, endoparasites, rodents, species diversity, taxonomic distinctness.
INTRODUCTION
Interactions between species within a community
include a variety of direct and indirect relations with
species exerting positive or negative eﬀects on each
other (Martin and Martin, 2001). Furthermore, facilitation and competition may operate among the
same species either simultaneously or with the
strength of each process varying in time or space
(Callaway and King, 1996 ; Callaway and Walker,
1997 ; Levine, 1999), with consequences on community organization. Recently, the many advantages
of using parasites to search for rules that govern
community organization have become clear. These
advantages include the ease of obtaining replicated
samples, the similar trophic and spatial niche of different parasite species, and the simultaneous presence on a host of several closely related parasites.
* Corresponding author : Ramon Science Center, P.O.
Box 194, Mizpe Ramon 80600, Israel. Tel: +972
8 6588764. Fax : +972 8 6586369. E-mail : krasnov@
bgu.ac.il
As a result, the number of studies of community
organization in parasitic organisms has increased
considerably (see Combes, 2001).
Depending on the presence or absence of interspeciﬁc interactions, both isolationist and interactive
parasite communities can be distinguished (Holmes
and Price, 1986 ; Bush et al. 1997). It is commonly
accepted that interactive communities are those that
comprise parasite species belonging to the same
guild, e.g. sharing the same trophic level, whereas
parasite species in isolationist communities, though
sharing a host, do not exploit the same resources
(Poulin, 1998). Nevertheless, interactions, although
rather indirect than direct, between parasite species
belonging to diﬀerent guilds are also possible. These
interactions could be mediated via host defence
mechanisms. Indeed, in contrast to the habitats of
free-living organisms, the habitat of parasites (host)
defends itself from exploiters (parasites) on ecological
time-scales. For example, suppression of a host defence system by one parasite species could lead to
greater opportunities for another parasite species to
survive and, thus, to facilitation among parasite
Parasitology (2005), 131, 557–568. f 2005 Cambridge University Press
doi:10.1017/S0031182005007912 Printed in the United Kingdom
B. R. Krasnov and others
species. Alternatively, the triggering of host defence
systems by one parasite species could lead to concomitant ﬁtness decrease in another parasite species.
An example of the latter is provided by the phenomenon of cross-resistance of a host against closelyrelated parasites. For instance, cross-resistance to
closely-related species of parasites has been repeatedly reported mainly for haematophagous arthropods (McTier, George and Bennet, 1981 ; Njau and
Nyiando, 1987 ; Khokhlova et al. 2004 a, b) but also
for protozoans (Leemans et al. 1999) and gastrointestinal helminths (Smith and Archibald, 1969).
However, haematophagy evolved independently in
diﬀerent taxa of arthropods and, thus, it is commonly
accepted that chemical mediators occurring in their
saliva are diﬀerent (Ribeiro, 1987, 1996 ; Jones, 1996).
Therefore, cross-resistance is expected against closely-related species but not against parasites belonging to diﬀerent taxa (Mans, Louw and Neitz, 2002).
Activation of an immune response and even maintenance of a competent immune system is an energetically demanding protective process that requires
trade-oﬀ decisions among competing energy demands for growth, reproduction, thermoregulation,
work, and immunity (Sheldon and Verhulst, 1996).
In other words, the trade-oﬀs occur between defence
against parasites and other concurrent needs of the
organism (Sheldon and Verhulst, 1996). Empirical
evidence suggests that such costs can be relatively
high (e.g., Moret and Schmid-Hempel, 2000 ;
Bonneaud et al. 2003). Development of immune responses and investment into immune defences should
thus depend on the pattern of parasite pressure (see
Combes, 2001 and references therein). For example,
it could depend on the frequency and probability
of parasite attacks (Martin et al. 2001 ; Tella,
Scheuerlein and Ricklefs, 2002). Consequently, if
the probability of attacks by parasites of one taxon is
higher than that by parasites of other taxa, a host
should develop those immune responses that are
most eﬀective against parasites belonging to a taxon
whose attacks are most probable (Khokhlova et al.
2004 b). Given (a) the likelihood of cross-resistance
against parasites belonging to the same taxon, and (b)
the likelihood of a trade-oﬀ between mounting
multiple immune responses and investment in other
functions, negative relationships between the species
diversity of diﬀerent parasite taxa within the same
host individual or population would be expected. A
host that eﬀectively withstands the attacks of, for
example, ﬂea parasites and is able to eliminate some
or even most of them could thus be more prone to the
attacks by, for example, various mite or tick species.
Furthermore, these negative relationships could be
expected in relation to both diﬀerent taxa of parasites
that share spatial and trophic level (e.g., haematophagous ectoparasites) and diﬀerent taxa of parasites
that belong to diﬀerent guilds (e.g., ectoparasitic
arthropods and gastrointestinal helminths). This is
558
because the defence properties of a host against
various parasites are based on the same morphological,
biochemical and energetic resources (immune
system).
On the other hand, also because of the common
basis of defence resources, suppression of host defence system due to parasitism by one parasite taxon
could facilitate parasitism by other parasite taxa, not
necessarily belonging to the same guild. In this case,
the species diversity of parasites of diﬀerent taxa
exploiting the same host individual or population
would be positively correlated.
However, in spite of extensive investigations of
community organization of parasites over the last 2
decades, most studies only considered interactions
(direct or mediated via host) within the same parasite
taxon or spatial and/or trophic guild (see Poulin,
1998 ; Combes, 2001 and references therein). One of
the reasons for this is a scarcity of data on parasites
belonging to diﬀerent taxa and/or guilds collected
from the same hosts in the same locality at the same
time, especially for terrestrial hosts. Studies that aim
to investigate the composition of communities of
both ecto- and endoparasites in terrestrial hosts are
especially rare.
Here we studied species diversity of 4 higher taxa of
haematophagous ectoparasites [ﬂeas (Siphonaptera),
sucking lice (Anoplura), mesostigmatid mites
(Mesostigmata) and ixodid ticks (Ixodidae)] and 4
higher taxa of gastrointestinal helminths [ﬂukes
(Trematoda), tapeworms (Cestoda), roundworms
(Nematoda) and thorny-headed worms (Acanthocephala)] in a variety of rodent hosts sampled in
diﬀerent localities of the world (Europe, Asia, North
and South America and Africa). The aim of this
study was to compare species diversity (a) between
parasite taxa sharing space and resources (diﬀerent
taxa of haematophagous parasites) and (b) between
parasite taxa that do not share space and resources
(ectoparasites and endoparasites) among diﬀerent
host species. We asked (a) whether there are relationships between the species diversity of diﬀerent
parasite taxa within the same host ; and (b) whether
these relationships (if any) are negative or positive.
The occurrence of relationships would advocate interactivity of the parasite community even if it is
composed of parasites from diﬀerent spatial and resource guilds. Negative relationships between the
species diversities of any 2 parasite taxa would suggest a trade-oﬀ between host defence mechanisms
aimed at diﬀerent parasites, whereas positive relationships would suggest host-mediated facilitation
among diﬀerent parasites.
In addition, rather than taking the mere number of
parasite species as a measure of species diversity, we
also applied a measure that takes into account the
taxonomic or phylogenetic aﬃnities of the various
parasite species (Clarke and Warwick, 1998, 1999 ;
Poulin and Mouillot, 2004). This measure places the
Facilitation among non-interactive parasite taxa
emphasis on the taxonomic distance between parasite
species exploiting a host rather than on their number.
MATERIALS AND METHODS
Data set
Data on ecto- and endoparasite species richness were
obtained from published studies that simultaneously
sampled either more than one of ectoparasite taxa
(ﬂeas, lice, mesostigmatid mites and ticks) or at least
one ectoparasite taxon and at least one taxon of gastrointestinal helminths and reported data on the
number and identity of parasite species found on a
particular rodent species in a particular location (see
Appendix, Table A1 and Table A2). We used only
those sources where sampling eﬀort (the number of
examined hosts) was reported. In total, we used data
on 80 rodent species for the analyses concerning ectoparasite taxa and 20 rodent species for the analysis
concerning ecto- versus endoparasites.
Estimates of parasite species richness may be biased
if some hosts are studied more intensively than others
(Morand and Poulin, 1998). Consequently, unequal
study eﬀort among host species may result in confounding variation in estimates of parasite species
richness. To ensure that variation in sampling eﬀort
did not bias estimates of species richness, we regressed the number of parasite species found against
the number of hosts examined. Parasite richness
appeared to be strongly aﬀected by sampling eﬀort
(r2=0.17–0.27, F=14.1–29.9, N=20–80 ; P<0.001
for all). Each value of parasite richness was then
substituted by its residual deviation from a linear
regression of the number of parasite species found
against the number of hosts examined in the ln-ln
space. This provided a measure of parasite richness
that is independent of sampling eﬀort.
Measures of parasite species diversity
We used 2 measures of parasite species diversity (a)
the number of parasite species found on a host species, or species richness, corrected for sampling eﬀort
(residuals of the linear regression against number of
hosts examined) and (b) average taxonomic distinctness (D+) of the parasite species present. When these
parasite species are placed within a taxonomic hierarchy, the average taxonomic distinctness is the mean
number of steps up the hierarchy that must be taken
to reach a taxon common to 2 parasite species, computed across all possible pairs of parasite species
(Clarke and Warwick, 1998, 1999 ; Warwick and
Clarke, 2001 ; Poulin and Mouillot, 2004). The
greater the taxonomic distinctness between parasite
species, the higher the number of steps needed, and
the higher the value of the index D+ (see details in
Poulin and Mouillot, 2004). All parasite species included here were ﬁtted into a taxonomic structure
with a diﬀerent number of hierarchical levels above
559
species, namely 8 for ﬂeas (subgenus or species
group, genus, tribe, subfamily, family, superfamily,
infraorder, and order), 4 for lice (genus, family,
suborder and order), 5 for mites (genus, family,
superfamily, cohort and suborder), 4 for ticks (subgenus, genus, subfamily and family) and 7 for
gastrointestinal helminths (genus, family, order, subclass, class, phylum and subkingdom). The sources
for taxonomic classiﬁcation were Smit (1982) and
Medvedev (1998) for ﬂeas, Durden and Musser
(1994) for sucking lice, Bregetova (1956), Halliday
(1998) and Salmane (2001) for mesostigmatid mites,
Camicas et al. (1998) and Horak, Camicas & Keirans
(2002) for ticks, and Dailey (1996) for helminths.
When ectoparasites of diﬀerent taxa were considered
together (for the analysis of species diversity between
ectoparasitic and endoparasitic assemblages), they
were ﬁtted into a taxonomic structure with 12 hierarchical levels above species (subgenus or species
group, genus, tribe, subfamily, family, superfamily,
cohort, infraorder or suborder, order, class and
phylum). The maximum value that the index D+ can
take is thus 4–12 (when all parasite species belong
to diﬀerent suborders/subfamilies-classes, respectively), and its lowest value is 1 (when all parasite
species belong to the same subgenus or species
group). However, since the index cannot be computed for hosts exploited by a single parasite species,
we assigned a D+ value of 0 to these host species, to
reﬂect their extremely species-poor parasite assemblages. To calculate D+, DM and RP have developed
a computer program using Borland C++ Builder 6.0
(available at http://www.otago.ac.nz/zoology/down
loads/poulin/TaxoBiodiv1.2). To compare taxonomic distinctness among diﬀerent parasite taxa we
scaled D+ values to range between 1 and 100, regardless of the number of taxonomic levels. Instead of
giving each step up the taxonomic tree a length value
of 1 unit, we gave it a length of 100/n, where n was the
maximum number of steps or taxonomic levels.
Across host species, the number of ectoparasite
species of a particular ectoparasite taxon exploiting a
host species was signiﬁcantly positively correlated
with D+ for this taxon (Pearson product-moment
correlations, r=0.68–0.88, N=38–74; respectively,
P<0.05 for all), indicating that this measure is inﬂuenced by the number of species in a host’s parasite
assemblage. However, D+ values for the assemblage
of combined ectoparasite taxa or intestinal helminths
were not aﬀected by the number of species in an assemblage (r=x0.01 and r=0.39, respectively; N=
20, P>0.05 for both). Therefore, in the subsequent
analyses D+ was corrected for the parasite species
richness in an assemblage when necessary.
Data analyses
To examine if the species diversity of an assemblage
of a particular parasite taxon within a host species is
B. R. Krasnov and others
560
Table 1. Pearson’s correlation coeﬃcients (r) for all pairwise associations
of species richness (SR) and taxonomic distinctness (D+) between
assemblages of four higher ectoparasite taxa found on the same host
species
(Both parameters were controlled for confounding variables (sampling eﬀort
in the case of SR, and number of species in the case of D+). In parentheses : value
of r after removal of 11 host species for which fewer than 10 individuals were
examined. *P<0.01.)
Taxon 1
Taxon 2
SR
D+
Fleas
Lice
Mesostigmatid mites
Ticks
Mesostigmatid mites
Ticks
Ticks
0.08 (0.08)
0.31* (0.32*)
0.47* (0.48*)
x0.03 (x0.03)
0.10 (0.10)
0.37* (0.36*)
x0.27 (x0.27)
0.10 (0.17)
0.07 (0.10)
x0.21 (x0.22)
0.06 (0.06)
0.18 (0.13)
Lice
Mesostigmatid
mites
associated with that of another parasite taxon, we
correlated species richness (corrected for sampling
eﬀort) and taxonomic distinctness (corrected for the
species richness of a parasite assemblage if necessary)
between each pair of ectoparasite taxa as well as
between the entire ectoparasite assemblage and the
entire assemblage of gastrointestinal helminths using
Pearson’s product-moment correlations. Because we
examined the correlations of the same ectoparasite
taxa in diﬀerent combinations, we avoided an inﬂated
Type I error by performing Bonferroni adjustments
of alpha. Signiﬁcance was only recorded at the adjusted level.
Treating host species as statistically independent
data points in a comparative study may be invalid
as it can introduce bias in the analysis (Harvey and
Pagel, 1991). To control for the eﬀects of phylogeny,
we used the method of independent contrasts
(Felsenstein, 1985). We used a phylogeny of rodents
derived from various sources (see Krasnov et al.
2004). To compute independent contrasts, we used
the PDAP : PDTREE program (Garland et al. 1993 ;
Midford, Garland and Maddison, 2004) implemented in Mesquite Modular System for Evolutionary Analysis (Maddison and Maddison, 2004).
Procedure of the method of independent contrasts
followed Garland, Harvey and Ives (1992). Regressions were forced through the origin as is standard
practice with contrasts, because of the arbitrariness
associated with the sign of independent contrasts (see
Garland et al. 1992 for details).
RESULTS
Comparison among ectoparasite taxa
Diﬀerent host species supported a diﬀerent number
of ectoparasites belonging to diﬀerent taxa. The number of ﬂea species per host species ranged from 1 to 19
with a median value of 2. Published surveys used in
this study reported no ﬂea species for 5 of 80 rodents
(Akodon azarae, Nectomys squamipes, Bolomys
lasiurus, Oryzomys subﬂavus, and Spermophilus beldingi). Lice were found on 38 of 80 rodent hosts only.
Species richness of these ectoparasites ranged from 1
(30 of 38 hosts) to a maximum of 3 species (4 of 38
hosts) with a median of 1. Of 80 rodent species, 68
were parasitized by mesostigmatid mites with the
number of species ranging from 1 to 21 with a median
of 4. Ticks were found on 55 of 80 rodents. Tick
species richness varied from one to 12 with a median
of 2. The species richness of ﬂea assemblages on a
host species varied signiﬁcantly across geographical
regions (Palaearctic, Nearctic, Neotropical and Afrotropical : ANOVA, F3,71=4.0, P<0.05) being highest in the Palaearctic. However, this signiﬁcance
disappeared when 3 of 27 Palaearctic species that
had the richest ﬂea assemblages (Alticola argentata,
Cricetulus migratorius and Microtus arvalis) were
excluded from the analysis (F3,68=2.6, P>0.05). On
the contrary, species richness of the assemblages of
other ectoparasite taxa did not diﬀer among regions
(ANOVAs, F3,34– 64=0.6–2.3, P>0.05 for all). The
same was true for taxonomic distinctness of the
assemblages of any ectoparasite taxon (ANOVAs,
F3,34–71=1.1–1.3, P>0.05 for all).
Numbers of species of most ectoparasite taxa on
the same host (controlled for sampling eﬀort) were
signiﬁcantly positively correlated with one another
(Table 1 ; see Fig. 1 for the illustrative example with
ﬂeas and ticks). However, this was not the case for
lice. The number of louse species was not correlated
with the number of species of any other ectoparasite
taxon (Table 1). Taxonomic distinctness (D+) was
not correlated among the assemblages of diﬀerent
ectoparasitic taxa (Table 1). The results did not
change after exclusion from the analyses of 11 host
species for which fewer than 10 individuals were
examined (Table 1).
Comparisons of species richness among ectoparasitic taxa using the method of independent
Number of tick species per host species
(controlled for sampling effort)
Facilitation among non-interactive parasite taxa
1·2
1·0
0·8
0·6
0·4
0·2
0·0
–0·2
–0·4
–0·6
–0·8
–1·0
–1·2 –1·0 –0·8 –0·6 –0·4 –0·2 0·0 0·2 0·4 0·6 0·8 1·0 1·2 1·4
Number of flea species per host species (controlled for
sampling effort)
Fig. 1. Relationships between the number of tick species
and the number of ﬂea species on the same host species
among 52 rodent species.
contrasts yielded essentially the same results as those
of conventional analyses. Species richness but not
taxonomic distinctness was signiﬁcantly positively
correlated among the assemblages of ﬂeas, mites and
ticks (Table 2), whereas neither the number of louse
species nor the taxonomic distinctness of their assemblages were correlated with those of other ectoparasites (Table 2). The results did not change after
exclusion from the analyses of 11 host species for
which fewer than 10 individuals were examined, as
was the case with conventional statistics (Table 1).
An illustrative example with mites and ticks is shown
in Fig. 2. The correlation remained signiﬁcant (r=
0.30, P<0.05) after removal of one data point from
the bottom left corner (contrast between Neotoma
ﬂoridana and Neotoma fuscipes) and two data points
from the upper right corner (contrast between
Alticola argentata and Alticola streltzovi and contrast
between Microtus arvalis and Microtus ochrogaster).
Comparison between ectoparasite and
endoparasites assemblages
Neither species richness nor taxonomic distinctness
of ectoparasite and endoparasite assemblages in a
host species diﬀered signiﬁcantly among geographical regions (ANOVAs, F2,17=0.2–1.3, P>0.05 for
all). The species richness of ectoparasite assemblages
was not correlated with that of the assemblage of
gastrointestinal helminths on the same host species
when their relationship was analysed using both
conventional statistics and the method of independent contrasts (r=0.26, N=20 and r=0.27, N=19,
respectively, P>0.05 for both). In contrast, the correlation between the taxonomic distinctness of ectoparasite assemblages and that of endoparasites was
highly signiﬁcantly positive when both conventional
analysis and the method of independent contrasts
were used (r=0.82, N=20 and r=0.83, N=19, respectively P<0.01 ; see Fig. 3 for independent contrasts). Correlations remained signiﬁcant after the
561
exclusion of 2 host species for which fewer than 10
individuals were examined (r=0.81, N=18 for
conventional analysis and r=0.84, N=17 for independent contrasts ; P<0.01 for both). In addition,
the correlation between independent contrasts in
taxonomic distinctness of ectoparasite assemblages
and independent contrasts in taxonomic distinctness
of assemblages of gastrointestinal helminths remained signiﬁcant, albeit weaker, when the two
right upper points (Fig. 3) were removed (r=0.47,
N=17, P<0.05) ; these points represented the
contrasts between Spermophilus armatus and
Spermophilus beldingi and between Geomys bursarius
and Perognathus parvus.
DISCUSSION
The results of this study demonstrated that, in general, the species diversities of diﬀerent parasite taxa
in the same host species are positively interrelated.
This appeared to be true among parasites that use the
same space and resource in their host (ﬂeas, mites and
ticks) as well as between parasites belonging to
completely diﬀerent spatial and trophic guilds (ectoparasites and gastrointestinal helminths). These results, combined with an earlier demonstration that
the species richnesses of diﬀerent groups of endoparasitic helminths covary among their vertebrate
hosts (Poulin and Morand, 2004, pp. 75–79), provide
strong evidence of apparent facilitation (sensu Levine,
1999) among diﬀerent parasite taxa.
The existence of relationships between species
diversities of diﬀerent parasite taxa (even those from
diﬀerent guilds) suggests that the host represents
an important force shaping parasite communities.
Moreover, positive correlations between species
diversities among 3 ectoparasite taxa and between
ecto- and endoparasites advocate host-mediated
facilitation among diﬀerent parasites. A host that
is unable to resist attacks from multiple ﬂea species
appears to be also unable to resist attacks from
multiple mite and tick species. When the diversity of
unrelated taxa of free-living organisms co-varies
positively across localities, the general explanation
usually invokes intrinsic diﬀerences in rates of colonization and extinction among localities (Gaston,
1996). It is thus possible that intrinsic properties of
the various host species could lead to some hosts
accumulating parasites of all taxa at a high rate. In
this context, our results are more likely due to some
biochemical or physiological properties of a host
rather than to its ecological characteristics. Indeed,
the depth and degree of complexity of a rodent burrow system can determine the relative richness of
ﬂea and mite assemblages (Kucheruk, 1983) because
pre-imaginal development in many species occurs
oﬀ-host. In most ixodid ticks, though, questing larvae and nymphs (adult ticks of most species parasitize mainly large mammals) do not depend on the
B. R. Krasnov and others
562
Table 2. Pearson’s correlation coeﬃcients (r) for all pairwise associations
of species richness (SR) and taxonomic distinctness (D+) between
assemblages of four higher ectoparasite taxa found on the same host
species using the method of phylogenetically independent contrasts
(Both parameters were controlled for confounding variables (sampling eﬀort
in the case of SR, and number of species in the case of D+). In parentheses : value
of r after removal of 11 host species for which fewer than 10 individuals were
examined. *P<0.01.)
Taxon 2
SR
D+
Fleas
Lice
Mesostigmatid mites
Ticks
Mesostigmatid mites
Ticks
Ticks
0.03 (0.04)
0.49* (0.48*)
0.58* (0.59*)
0.28 (0.29)
0.31 (0.31)
0.50* (0.43*)
x0.29 (x0.29)
x0.07 (x0.03)
0.08 (0.11)
x0.21 (0.22)
0.12 (0.12)
0.17 (0.16)
Lice
Contrasts in the number of tick species
per host species (controlled for sampling effort)
Mesostigmatid mites
1·0
0·8
0·6
0·4
0·2
0·0
–0·2
–0·4
–0·6
–0·8
–1·0
–1·4 –1·2 –1·0 –0·8 –0·6 –0·4 –0·2 0·0 0·2 0·4 0·6 0·8 1·0 1·2
Contrasts in the number of mite species per host species
(controlled for sampling effort)
Contrasts in the taxonomic distinctness
of ectoparasite assemblages
Taxon 1
3·5
3·0
2·5
2·0
1·5
1·0
0·5
0·0
–0·5
–1·0
–1·5
–0·3
–0·2
–0·1
0·0
0·1
0·2
0·3
0·4
Contrasts in the taxonomic distinctness of endoparasite
assemblages
Fig. 2. Relationships between the number of tick species
and the number of mesostigmatid mite species on the
same host species among 55 rodent species using
independent contrasts.
Fig. 3. Relationships between the taxonomic distinctness
of ectoparasite and endoparasite assemblages among 20
rodent species using phylogenetically independent
contrasts.
host’s burrow but crawl up the stems of grass or
perch on the edges of leaves on the ground and wait
for a host passing by.
On the other hand, a host species that is able to
resist attacks from many species of one parasite taxon
appears to be able also to resist attacks from many
species of other parasite taxa. This suggests some
level of cross-resistance against distantly related
parasites. In particular, rodent species that are exploited by only a few ﬂea species appeared also to be
exploited by only few mite and tick species. Although
many chemical mediators that are contained in the
saliva of diﬀerent ectoparasite lineages are diﬀerent
(Ribeiro, 1996), some salivary anti-clotting, antiplatelet and vasodilatory substances can be quite
similar among taxa. Indeed, cross-immunity between distantly-related parasite taxa has been reported. For example, rabbits infested with mites
Prosoptes cuniculi produce antibodies reactive to both
mite and tick extracts (den Hollander and Allen,
1986). However, the occurrence of cross-immunity
seems to depend on both parasite and host taxon. For
example, guinea pigs demonstrated cross-immunity
between diﬀerent ticks of the genus Dermacentor but
not between ticks of the genera Dermacentor and
Amblyomma (McTier et al. 1981). Rabbits demonstrated cross-resistance between 2 Hyalomma ticks
(Kumar and Kumar, 1996), but not between
Rhipicephalus and Ixodes (Rechav, Heller-Haupt and
Varma, 1989). Cross-immunity between 2 Rhipicephalus species was reported for rabbits (Njau and
Nyindo, 1987), but not for guinea pigs (Rechav et al.
1989). Nevertheless, close homology of saliva proteins was found in closely related argasid ticks (Mans
et al. 2002) but not in closely-related sand ﬂies
(Warburg et al. 1994). Thus, some still unknown
factors determine cross-resistance patterns in different host–parasite systems.
Species richness of anopluran lice was not correlated with that of any other ectoparasite taxon,
whereas their taxonomic distinctness was sometimes
even negatively, albeit not signiﬁcantly, correlated
with that of other taxa. The number of louse species
on a host species was low independently of the species
Facilitation among non-interactive parasite taxa
richness of any other parasite taxon. Indeed, the vast
majority of host species harboured a single louse
species only. Furthermore, taxonomic distinctness of
louse assemblages was always low (in average across
hosts, 12.4¡4.0 compared with 54.4¡4.3, 41.7¡2.8
and 48.8¡5.3 for ﬂeas, mites and ticks, respectively)
regardless of whether the D+ of other ectoparasite
taxa is high or low. In other words, some ectoparasite
taxa (e.g., lice) could be constrained in their taxonomic diversity, whereas this is not the case for other
taxa. Constraints in louse taxonomic diversity can be
explained by the extremely high host speciﬁcity of lice
and their extremely low dispersal capacity. Another
explanation can be that sucking lice were undersampled in at least part of the reported surveys. This
is likely the case because these insects are small,
usually attach to the hair bases next to the host skin
and, thus, cannot be easily brushed oﬀ the host.
The positive relationships among species diversities of the assemblages of diﬀerent ectoparasites as
well as between ecto- and endoparasites could arise
also from immunodepression in a host subjected to
multiple immune challenges from a variety of parasite species. The occurrence of a positive correlation
in terms of taxonomic distinctness rather than in
terms of number of species between ecto- and endoparasite assemblages strengthens this explanation.
Immunity is an energetically and/or nutritionally
demanding process (Lochmiller and Deerenberg,
2000). Indeed, relationships between parasitism,
immunity and reproduction observed in wild birds
and mammals strongly support a high energy cost of
the immune system (Norris, Anwar and Read, 1994 ;
Demas and Nelson, 1998 ; Ilmonen et al. 2003). The
diﬀerence between defence mechanisms against
haematophagous ectoparasites versus intestinal helminths is much sharper than that between defence
mechanisms against diﬀerent ectoparasite taxa (see
Wakelin, 1996 ; Wikel, 1996). Maintaining several
diﬀerent means of defence is likely more costly than
mounting one speciﬁc type of defence (Taylor,
Mackinnon and Read, 1998). As a result, the eﬀectiveness of energy allocation to immune defence decreases as the diversity of attack types increases
(Jokela, Schmid-Hempel and Rigby, 2000). Jokela
et al. (2000) argued that in cases when the diversity of
attacks is high and, thus, the eﬀectiveness of defence
is low, the optimal strategy is to tolerate damage.
Consequently, a host subjected to attacks from
multiple parasite species is forced to give up its defence and to surrender. This can be one of the reasons
explaining why hosts that are exploited by taxonomically diverse assemblages of haematophagous
arthropods, also harbour assemblages of gastrointestinal helminths of high taxonomic distinctness.
Another, not necessarily alternative, explanation
for the observed patterns is that host species can diﬀer
also in their intrinsic ability to defend themselves
against parasites using their immune system.
563
Diﬀerent, sometimes even closely related, rodent
species have been shown to have diﬀerent abilities to
mount both humoral and cell-mediated immune responses (Klein and Nelson, 1998 a, b). As a result, a
rodent with lower intrinsic immunocompetence can
be exploited by a higher number of parasite species
compared with more immunocompetent species.
Finally, the results of this study do not support
suggestions of strong direct or host-mediated competitive exclusion between diﬀerent parasite species
or lineages (Waage, 1979 ; Rozsa, 1993), although
such competition undoubtedly occurs (Barker and
Close, 1990 ; Patrick, 1991 ; Combes, 2001). Instead,
our results suggest host-mediated facilitation among
species of diﬀerent taxa within parasite assemblages
of rodent hosts. Because a host is not only a resource
but also a competitor for a parasite (Combes, 2001),
the relationships among diﬀerent parasite lineages in
a host species represent a sort of apparent facilitation,
i.e. positive interactions mediated by a shared competitor (Levine, 1999). Apparent facilitation is considered as an important process in communities of
both free-living (Levine, 1999) and parasitic (Cox,
2001 ; Krasnov et al. 2005) organisms.
This study was partly supported by the Israel Science
Foundation (Grant no. 249/04 to B. Krasnov, I.
Khokhlova and G. Shenbrot) and by Israel Ministry
of Science and Technology. We thank two anonymous
referees for helpful comments. This is publication no. 178
of the Ramon Science Center and no. 483 of the Mitrani
Department of Desert Ecology.
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APPENDIX
Table A1. Data on rodents and their ectoparasites included in the analyses of parasite species diversity
among higher ectoparasite taxa
Species
Aethomys chrysophilus
Akodon arviculoides
Akodon azarae
Akodon montensis
Akodon serrensis
Allactaga elater
Alticola argentata
Alticola streltzovi
Ammospermophilus leucurus
Number of
examined individuals
46
11
17
4
14
51
201
800
14
Number of
parasite species
Source
7
8
4
7
8
11
29
18
11
Braack et al. 1996
Lopes, Linardi and Botelho, 1989
Nava, Lareschi and Voglino, 2003
Barros-Battesti et al. 1998
Barros-Battesti et al. 1998
Sartbaev, 1975
Sartbaev, 1975
Shubin, 1959
Jenkins and Grundmann, 1973
B. R. Krasnov and others
566
Table A1. (Cont.)
Species
Number of
examined individuals
Number of
parasite species
Source
Apodemus uralensis
Arvicanthis niloticus
Arvicola terrestris
Bolomys lasiurus
Callosciurus erythraeus
Clethrionomys glareolus
Clethrionomys rutilus
Cricetulus barabensis
Cricetulus migratorius
Dryomys nitedula
Ellobius talpinus
Eutamis sibiricus
Geomys bursarius
Gerbillus andersoni
Glaucomys volans
Holochilus brasiliensis
Lasiopodomys brandti
Lemniscomys striatus
Marmota baibacina
Marmota sibirica
Mastomys natalensis
Meriones erythrourus
Meriones tamariscinus
Microtus arvalis
Microtus fortis
Microtus gregalis
Microtus ochrogaster
Microtus oeconomus
Mus musculus
Napaeozapus insignis
Nectomys squamipes
Neoﬁber alleni
Neotoma cinerea
Neotoma ﬂoridana
Neotoma fuscipes
Ochrotomys nuttali
Oligoryzomys delticola
Oligoryzomys ﬂavescens
Ondatra zibethica
Oryzomys nigripes
Oryzomys palustris
Oryzomys russatus
Oryzomys subﬂavus
Oryzomys utiaritensis
Oxymycterus rufus
Oxymycterus rutilans
Pedetes capensis
Perognatus parvus
Peromyscus gossypinus
Peromyscus leucopus
Peromyscus maniculatus
Proechimys iheringi
Rattus turkestanicus
Reithrodontomys megalotis
Scapteromus aquaticus
Sciurus carolinensis
Sciurus niger
Sciurus vulgaris
Sicista tjanschanica
Sigmodon hispidus
Spermophilus armatus
Spermophilus beldingi
Spermophilus fulvus
Spermophilus lateralis
Spermophilus relictus
1334
6
1103
4
105
65
309
6
133
127
113
5
144
240
70
7
171
7
266
1458
14
152
502
416
277
846
59
5
461
101
11
25
30
47
35
46
10
8
85
9
11
139
10
33
29
4
118
183
64
60
28
75
391
24
22
14
87
11
195
23
14
12
668
24
176
52
3
37
4
3
16
22
11
40
6
14
8
4
9
9
5
21
5
16
7
6
25
35
43
7
46
9
11
20
5
2
3
19
12
12
12
8
6
4
6
2
6
5
14
8
4
7
3
9
10
7
3
21
2
5
3
6
4
21
7
17
1
5
17
8
Sartbaev, 1975
Oguge, Rerieya and Ondiaka, 1997
Letova, Emelyanova and Letov, 1963
Lopes et al. 1989
Shinozaki et al. 2004
Bugmyrin et al. 2003
Elshanskaya and Popov, 1972
Shvedko, 1958
Sartbaev, 1975
Sartbaev, 1975
Sartbaev, 1975
Elshanskaya and Popov, 1972
Bartel and Gardner, 2000
Lehmann, 1992
Pung et al. 2000
Nava et al. 2003
Vasiliev, 1966
Oguge et al. 1997
Sartbaev, 1975
Vasiliev, 1966
Oguge et al. 1997
Sartbaev, 1975
Sartbaev, 1975
Sartbaev, 1975
Garbuzov, 1958
Sartbaev, 1975
Ritzi and Whitaker, 2003
Elshanskaya and Popov, 1972
Sartbaev, 1975
Whitaker, 1963 a
Bossi, Linhares and de Godoy Bergallo, 2002
Smith, Whitaker and Layne, 1988
Cudmore, 1986
Durden et al. 1997
Cudmore, 1986
Durden et al. 2004
Lareschi et al. 2003
Nava et al. 2003
Garbuzov, 1958
Barros-Battesti et al. 1998
Kollars, Durden and Oliver, 1997
Bossi et al. 2002
Lopes et al. 1989
Lopes et al. 1989
Lareschi et al. 2003
Linardi et al. 1991
Anderson and Kok, 2003
O’Farrel, 1975
Durden et al. 2000
Ritzi and Whitaker, 2003
Ritzi and Whitaker, 2003
Bossi et al. 2002
Sartbaev 1975
Kollars et al. 1997
Nava et al. 2003
Kollars et al. 1997
Coyner, Wooding and Forrester, 1996
Sartbaev, 1975
Sartbaev, 1975
Durden et al. 2000
Jenkins and Grundmann, 1973
Jenkins and Grundmann, 1973
Sartbaev, 1975
Jenkins and Grundmann, 1973
Sartbaev, 1975
Facilitation among non-interactive parasite taxa
567
Table A1. (Cont.)
Species
Spermophilus townsendi
Spermophilus undulatus
Spermophilus variegatus
Synaptomys cooperi
Tatera leucogaster
Zapus hudsonius
Number of
examined individuals
25
39
61
15
46
956
Number of
parasite species
Source
7
9
14
9
9
9
Jenkins and Grundmann, 1973
Elshanskaya and Popov, 1972
Jenkins and Grundmann, 1973
Ritzi and Whitaker, 2003
Braack et al. 1996
Whitaker, 1963 b
Table A2. Data on rodents and their ecto- (EC) and endoparasites (EN) included in the analyses
of parasite species diversity between ectoparasites and endoparasites
Number of individuals
examined
Number of species
Species
EC
EN
EC
EN
Source
Alticola streltzovi
Ammospermophilus leucurus
Ammospermophilus nelsoni
Arvicanthis niloticus
Clethrionomys glareolus
Cricetulus barabensis
Geomys bursarius
Glaucomys volans
Lemniscomys striatus
Mastomys natalensis
Napaeozapus insignis
Perognatus parvus
Rattus norvegicus
800
14
500
6
65
63
144
70
7
14
101
183
255
200
135
37
6
65
63
144
70
7
14
113
38
255
18
11
3
3
16
11
4
9
5
6
5
3
4
3
9
4
3
10
4
8
5
4
5
4
3
7
Sciurus niger
Spermophilus armatus
Spermophilus beldingi
Spermophilus lateralis
Spermophilus townsendi
Spermophilus variegatus
Zapus hudsonius
87
14
12
24
25
61
956
119
35
12
100
12
154
956
6
17
1
17
7
14
10
11
6
4
6
2
17
7
Shubin, 1959
Jenkins and Grundmann, 1973
Hawbecker, 1959
Oguge et al. 1997
Bugmyrin et al. 2003
Letov et al. 1966
Bartel and Gardner, 2000
Pung et al. 2000
Oguge et al. 1997
Oguge et al. 1997
Whitaker, 1963 a
O’Farrel, 1975
Stojcevic, Mihaijlevic and
Marunculic, 2004
Coyner, Wooding and Forrester, 1996
Jenkins and Grundmann, 1973
Jenkins and Grundmann, 1973
Jenkins and Grundmann, 1973
Jenkins and Grundmann, 1973
Jenkins and Grundmann, 1973
Whitaker, 1963 b
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